Mechanisms in colistin-resistant superbugs transmissible from veterinary, livestock and animal food products to humans

Document Type : Review article

Authors

1 Ph.D. in Pharmaceutical Biotechnology, Stem Cells and Regenerative Medicine Innovation Center, Kerman University of Medical Sciences, Kerman, Iran

2 Graduated from College of Basic Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran

3 Department of Pathological Analysis, College of Applied Medical Sciences, University of Karbala, Karbala, Iraq

4 Ph.D. in Bacteriology, Stem Cells and Regenerative Medicine Innovation Center, Kerman University of Medical Sciences, Kerman, Iran

5 Department of Pharmacy, School of Pharmacy, Hamadan University of Medical Sciences, Hamadan, Iran

6 Department of Microbiology, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran

Abstract

In the era of antibiotic resistance, where multidrug-resistant (MDR), extensively drug resistant (XDR), and pan-drug resistant (PDR) Gram-negative infections are prevalent, it is crucial to identify the primary sources of antibiotic resistance, understand resistant mechanisms, and develop strategies to combat these mechanisms. The emergence of resistance to last-resort antibiotics like colistin has sparked a war between humanity and resistant bacteria, leaving humanity struggling to find effective countermeasures. Although colistin is used as a highly toxic antibiotic in infections that are not treated with routine antibiotics, its widespread use in animal breeding and veterinary medicine has contributed to the spread of colistin-resistant bacteria, plasmid-borne colistin resistance genes (mcr), and antibiotic residues in livestock and animal-derived foods. These sources can potentially transmit colistin resistance to humans through various routes. Therefore, managing the use of colistin in livestock and animal foods, implementing strict monitoring, and establishing guidelines for its proper use are essential to prevent the escalation of colistin resistance. This review article discusses the latest mechanisms of colistin antibiotic resistance, particularly biofilm production as a public health threat, the livestock and animal food sources of this resistance, and the routes of transmission to humans.

Keywords

Main Subjects

References

Abuoun, M; Stubberfield, EJ; Duggett, NA; Kirchner, M; Dormer, L; Nunez-Garcia, J; Randall, LP; Lemma, F; Crook, DW and Teale, C (2017). mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J. Antimicrob. Chemother., 72: 2745-2749.
Azimi, L and Lari, AR (2019). Colistin-resistant Pseudomonas aeruginosa clinical strains with defective biofilm formation. GMS HIC., 14: 134-151.
Barlaam, A; Parisi, A; Spinelli, E; Caruso, M; Taranto, PD and Normanno, G (2019). Global emergence of colistin-resistant Escherichia coli in food chains and associated food safety implications: a review. J. Food Prot., 82: 1440-1448.
Bastidas-Caldes, C; De Waard, JH; Salgado, MS; Villacís, MJ; Coral-Almeida, M; Yamamoto, Y and Calvopiña, M (2022). Worldwide prevalence of mcr-mediated colistin-resistance Escherichia coli in isolates of clinical samples, healthy humans, and livestock—a systematic review and meta-analysis. Pathogens. 11: 659-668.
Binsker, U; Oelgeschläger, K; Neumann, B; Werner, G; Käsbohrer, A and Hammerl, JA (2023). Genomic evidence of mcr-1.26 IncX4 plasmid transmission between poultry and humans. Microbiol. Spectr., 11: e01015-e01023.
Biswas, U; Das, S; Barik, M and Mallick, A (2024). Situation report on mcr-carrying colistin-resistant clones of enterobacterales: A global update through human-animal-environment interfaces. Curr. Microbiol., 81: 12-26.
Borowiak, M; Fischer, J; Hammerl, JA; Hendriksen, RS; Szabo, I and Malorny, B (2017). Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. J. Antimicrob. Chemother., 72: 3317-3324.
Carattoli, A; Villa, L; Feudi, C; Curcio, L; Orsini, S; Luppi, A; Pezzotti, G and Magistrali, CF (2017). Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill., 22: 30589.
Centres for Disease Control and Prevention (2013) Antibiotic resistance threats in the United States. https:// www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf. Accessed 17 July 2017.
Chegini, Z; Khoshbayan, A; Taati Moghadam, M; Farahani, I; Jazireian, P and Shariati, A (2020). Bacteriophage therapy against Pseudomonas aeruginosa biofilms: A review. Ann. Clin. Microbiol. Antimicrob., 19: 1-17.
Cheung, J; Bingman, CA; Reyngold, M; Hendrickson, WA and Waldburger, CD (2008). Crystal structure of a functional dimer of the PhoQ sensor domain. J. Biol. Chem., 283: 13762-13770.
Dafopoulou, K; Xavier, BB; Hotterbeekx, A; Janssens, L; Lammens, C; Dé, E; Goossens, H; Tsakris, A; Malhotra-Kumar, S and Pournaras, S (2015). Colistin-resistant Acinetobacter baumannii clinical strains with deficient biofilm formation. Antimicrob. Agents Chemother., 60: 1892-1895.
Dandachi, I; Fayad, E; El-Bazzal, B; Daoud, Z and Rolain, JM (2019). Prevalence of extended-spectrum beta-lactamase-producing Gram-negative bacilli and emergence of mcr-1 colistin resistance gene in Lebanese swine farms. Microb. Drug Resist., 25: 233-240.
Delannoy, S; Le Devendec, L; Jouy, E; Fach, P; Drider, D and Kempf, I (2017). Characterization of colistin-resistant Escherichia coli isolated from diseased pigs in France. Front. Microbiol., 8: 2278-2285.
Dousari, AS and Satarzadeh, N (2021). The spread of carbapenemase genes in Klebsiella pneumoniae in Iran: a Systematic Review. Int. J. Bas. Sci. Med., 6: 1-10.
El-Sayed Ahmed, MAEG; Zhong, LL; Shen, C; Yang, Y; Doi, Y and Tian, GB (2020). Colistin and its role in the Era of antibiotic resistance: an extended review (2000-2019). Emerg. Micro. Infec., 9: 868-885.
Farshadzadeh, Z; Taheri, B; Rahimi, S; Shoja, S; Pourhajibagher, M; Haghighi, MA and Bahador, A (2018). Growth rate and biofilm formation ability of clinical and laboratory-evolved colistin-resistant strains of Acinetobacter baumannii. Front. Microbiol., 9: 153-167.
García-Meniño, I; Díaz-Jiménez, D; García, V; De Toro, M; Flament-Simon, SC; Blanco, J and Mora, A (2019). Genomic characterization of prevalent mcr-1, mcr-4, and mcr-5 Escherichia coli within swine enteric colibacillosis in Spain. Front. Microbiol., 10: 2469-2478.
Ghimire, L; Singh, DK; Basnet, HB; Bhattarai, RK; Dhakal, S and Sharma, B (2014). Prevalence, antibiogram and risk factors of thermophilic Campylobacter spp. in dressed porcine carcass of Chitwan, Nepal. BMC Microbiol., 14: 1-7.
Güzel, M; Avsaroglu, MD and Soyer, Y (2020). Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015. Food and Health. 6: 160-169.
Hassen, B; Saloua, B; Abbassi, MS; Ruiz-Ripa, L; Mama, OM; Hassen, A; Hammami, S and Torres, C (2019). mcr-1 encoding colistin resistance in CTX-M-1/CTX-M-15-producing Escherichia coli isolates of bovine and caprine origins in Tunisia. First report of CTX-M-15-ST394/D E. coli from goats. Comp. Immunol. Microbiol. Infect. Dis., 67: 101366-101377.
Hémonic, A; Chauvin, C and Corrégé, I (2014). Antibiotic uses in pig farming: reasons and associated therapeutic strategies. J. Rech. Porci., 46: 135-140.
Hu, Y; Fanning, S; Gan, X; Liu, C; Nguyen, S; Wang, M; Wang, W; Jiang, T; Xu, J and Li, F (2019). Salmonella harbouring the mcr-1 gene isolated from food in China between 2012 and 2016. J. Antimicrob. Chemother., 74: 826-828.
Huang, J; Li, C; Song, J; Velkov, T; Wang, L; Zhu, Y and Li, J (2020). Regulating polymyxin resistance in Gram-negative bacteria: roles of two-component systems PhoPQ and PmrAB. Future. Microbiol., 15: 445-459.
Huang, X; Yu, L; Chen, X; Zhi, C; Yao, X; Liu, Y; Wu, S; Guo, Z; Yi, L and Zeng, Z (2017). High prevalence of colistin resistance and mcr-1 gene in Escherichia coli isolated from food animals in China. Front. Microbiol., 8: 562-578.
Ilbeigi, K; Askari Badouei, M; Vaezi, H; Zaheri, H; Aghasharif, S and Kafshdouzan, K (2021). Molecular survey of mcr1 and mcr2 plasmid mediated colistin resistance genes in Escherichia coli isolates of animal origin in Iran. BMC Res. Notes. 14: 1-5.
Irrgang, A; Roschanski, N; Tenhagen, BA; Grobbel, M; Skladnikiewicz-Ziemer, T; Thomas, K; Roesler, U and Kaesbohrer, A (2016). Prevalence of mcr-1 in E. coli from livestock and food in Germany, 2010-2015. PloS One. 11: e0159863-e0159871.
Jansen, W; Van Hout, J; Wiegel, J; Iatridou, D; Chantziaras, I and De Briyne, N (2022). Colistin use in european livestock: Veterinary field data on trends and perspectives for further reduction. J. Vet. Sci., 9: 650-658.
Kiaei, S; Moradi, M; Nave, HH; Hashemizadeh, Z; Taati-Moghadam, M and Kalantar-Neyestanaki, D (2019). Emergence of co-existence of bla NDM with rmtC and qnrB genes in clinical carbapenem-resistant Klebsiella pneumoniae isolates in burning center from southeast of Iran. Folia. Microbiol., 64: 55-62.
Kim, S; Woo, JH; Kim, N; Kim, MH; Kim, SY; Son, JH; Moon, DC; Lim, SK; Shin, M and Lee, JC (2019). Characterization of chromosome-mediated colistin resistance in Escherichia coli isolates from livestock in Korea. Infect. Drug. Resist., 12: 3291-3303.
Klinger-Strobel, M; Stein, C; Forstner, C; Makarewicz, O and Pletz, MW (2017). Effects of colistin on biofilm matrices of Escherichia coli and Staphylococcus aureus. Int. J. Antimicrob. Agents. 49: 472-479.
Kumar, H; Chen, BH; Kuca, K; Nepovimova, E; Kaushal, A; Nagraik, R; Bhatia, SK; Dhanjal, DS; Kumar, V and Kumar, A (2020). Understanding of colistin usage in food animals and available detection techniques: a review. J. Anim., 10: 1892-1904.
Lay, KK; Jeamsripong, S; Sunn, KP; Angkititrakul, S; Prathan, R; Srisanga, S and Chuanchuen, R (2021). Colistin resistance and ESBL production in Salmonella and Escherichia coli from pigs and pork in the Thailand, Cambodia, Lao PDR, and Myanmar border area. J. Antibiot., 10: 657-670.
Le, PQ; Awasthi, SP; Hatanaka, N; Hinenoya, A; Hassan, J; Ombarak, RA; Iguchi, A; Tran, NTT; Dao, KVT and Vien, MQ (2021). Prevalence of mobile colistin resistance (mcr) genes in extended-spectrum β-lactamase-producing Escherichia coli isolated from retail raw foods in Nha Trang, Vietnam. Int. J. Food Microbiol., 346: 109164-109177.
Lemlem, M; Aklilu, E; Mohamed, M; Kamaruzzaman, NF; Zakaria, Z; Harun, A; Devan, SS; Kamaruzaman, INA; Reduan, MFH and Saravanan, M (2023). Phenotypic and genotypic characterization of colistin-resistant Escherichia coli with mcr-4, mcr-5, mcr-6, and mcr-9 genes from broiler chicken and farm environment. BMC Microbiol., 23: 392-405.
Li, XP; Fang, LX; Song, JQ; Xia, J; Huo, W; Fang, JT; Liao, XP; Liu, YH; Feng, Y and Sun, J (2016). Clonal spread of mcr-1 in PMQR-carrying ST34 Salmonella isolates from animals in China. Sci. Rep., 6: 1-8.
Lin, J; Xu, C; Fang, R; Cao, J; Zhang, X; Zhao, Y; Dong, G; Sun, Y and Zhou, T (2019). Resistance and heteroresistance to colistin in Pseudomonas aeruginosa isolates from Wenzhou, China. Antimicrob. Agents Chemother., 63: e00556-19.
Liu, G; Ali, T; Gao, J; Ur Rahman, S; Yu, D; Barkema, HW; Huo, W; Xu, S; Shi, Y and Kastelic, JP (2020). Co-occurrence of plasmid-mediated colistin resistance (mcr-1) and extended-spectrum β-lactamase encoding genes in Escherichia coli from bovine mastitic milk in China. Microb. Drug Resist., 26: 685-696.
Lu, X; Zhang, P; Du, P; Zhang, X; Wang, J; Yang, Y; Sun, H; Wang, Z; Cui, S and Li, R (2023). Prevalence and genomic characteristics of mcr-positive Escherichia coli strains isolated from humans, pigs, and foods in China. Microbiol. Spectr., 11: e04569-e04622.
Martínez-Servat, S; Yero, D; Huedo, P; Marquez, R; Molina, G; Daura, X and Gibert, I (2018). Hetero-geneous colistin-resistance phenotypes coexisting in Stenotrophomonas maltophilia isolates influence colistin susceptibility testing. Front. Microbiol., 9: 2871-2879.
Mirshekar, M; Zadeh, RG; Moghadam, MT; Shahbazi, S and Jazi, FM (2024). Upregulation of pmrA, pmrB, pmrC, phoQ, phoP, and arnT genes contributing to resistance to colistin in superbug Klebsiella pneumoniae isolates from human clinical samples in Tehran, Iran. New Microb. New Infect., 59: 101275-101287.
Moghadam, MT; Amirmozafari, N; Shariati, A; Hallajzadeh, M; Mirkalantari, S; Khoshbayan, A and Jazi, FM (2020). How phages overcome the challenges of drug resistant bacteria in clinical infections. Infect. Drug. Resist., 13: 45-61.
Moghadam, MT; Chegini, Z; Khoshbayan, A; Farahani, I and Shariati, A (2021a). Helicobacter pylori biofilm and new strategies to combat it. Curr. Mol. Med., 21: 549-561.
Moghadam, MT; Chegini, Z; Norouzi, A; Dousari, AS and Shariati, A (2021b). Three-decade failure to the eradication of refractory Helicobacter pylori infection and recent efforts to eradicate the infection. Curr. Pharm. Biotechnol., 22: 945-959.
Moghadam, MT; Mojtahedi, A; Moghaddam, MM; Fasihi-Ramandi, M and Mirnejad, R (2022). Rescuing humanity by antimicrobial peptides against colistin-resistant bacteria. Appl. Microbiol. Biotechnol., 106: 3879-3893.
Moghadam, MT; Mojtahedi, A; Salamy, S; Shahbazi, R; Satarzadeh, N; Delavar, M and Ashoobi, MT (2024). Phage therapy as a glimmer of hope in the fight against the recurrence or emergence of surgical site bacterial infections. J. Infect., 32: 1-18.
Mohebi, S; Golestani-Hotkani, Z; Foulad-Pour, M; Nazeri, P; Mohseni, F; Hashemizadeh, Z; Moghani-Bashi, Z; Niksefat, N; Rastegar, S and Khajedadian, M (2023). Characterization of integrons, extended spectrum beta lactamases and genetic diversity among uropathogenic Escherichia coli isolates from Kerman, south east of Iran. Iran. J. Microbiol., 15: 616-628.
Mousavi, SM; Babakhani, S; Moradi, L; Karami, S; Shahbandeh, M; Mirshekar, M; Mohebi, S and Moghadam, MT (2021). Bacteriophage as a novel therapeutic weapon for killing colistin-resistant multi-drug-resistant and extensively drug-resistant Gram-negative bacteria. Curr. Microbiol., 56: 1-14.
Obaidat, M; Tarazi, YH and Alsmadi, WM (2022). Individual and herd-level prevalences and antimicrobial resistance of plasmid-mediated colistin resistance Escherichia coli in small ruminant’s dairy farms in Jordan. Papers. Available at SSRN 4022967.
Odoi, JO; Takayanagi, S; Sugiyama, M; Usui, M; Tamura, Y and Asai, T (2021). Prevalence of colistin-resistant bacteria among retail meats in Japan. J. Food. Saf., 9: 48-56.
Olaitan, AO; Thongmalayvong, B; Akkhavong, K; Somphavong, S; Paboriboune, P; Khounsy, S; Morand, S and Rolain, JM (2015). Clonal transmission of a colistin-resistant Escherichia coli from a domesticated pig to a human in Laos. J. Antimicrob. Chemother., 70: 3402-3404.
Palupi, MF; Wibawan, IWT; Sudarnika, E; Maheshwari, H and Darusman, HS (2019). Prevalence of mcr-1 colistin resistance gene in Escherichia coli along broiler meat supply chain in Indonesia. Biotropia. 26: 272126-272138.
Panta, PR; Kumar, S; Stafford, CF; Billiot, CE; Douglass, MV; Herrera, CM; Trent, MS and Doerrler, WT (2019). A DedA family membrane protein is required for Burkholderia thailandensis colistin resistance. Front. Microbiol., 10: 2532-2548.
Park, NH; Lee, SJ; Lee, EB; Birhanu, BT and Park, SC (2021). Colistin induces resistance through biofilm formation, via increased phoQ expression, in avian pathogenic Escherichia coli. J. Pathog., 10: 1525-1537.
Poirel, L; Jayol, A and Nordmann, P (2017). Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin. Microbiol. Rev., 30: 557-596.
Poirel, L; Madec, JY; Lupo, A; Schink, AK; Kieffer, N; Nordmann, P and Schwarz, S (2018). Antimicrobial resistance in Escherichia coli. Antimicrobial resistance in bacteria from livestock and companion animals. Microbiol. Spectr., 153: 289-316.
Poulikakos, P; Tansarli, G and Falagas, M (2014). Combination antibiotic treatment versus monotherapy for multidrug-resistant, extensively drug-resistant, and pandrug-resistant Acinetobacter infections: a systematic review. Eur. J. Clin. Microbiol., 33: 1675-1685.
Quesada, A; Porrero, MC; Téllez, S; Palomo, G; García, M and Domínguez, L (2015). Polymorphism of genes encoding PmrAB in colistin-resistant strains of Escherichia coli and Salmonella enterica isolated from poultry and swine. J. Antimicrob. Chemother., 70: 71-74.
Rastegar, S; Skurnik, M; Niaz, H; Tadjrobehkar, O; Samareh, A; Hosseini-Nave, H and Sabouri, S (2024a). Isolation, characterization, and potential application of Acinetobacter baumannii phages against extensively drug-resistant strains. Virus Genes. 78: 1-12.
Rastegar, S; Skurnik, M; Tadjrobehkar, O; Samareh, A; Samare-Najaf, M; Lotfian, Z; Khajedadian, M; Hosseini-Nave, H and Sabouri, S (2024b). Synergistic effects of bacteriophage cocktail and antibiotics combinations against extensively drug-resistant Acinetobacter baumannii. BMC Infect. Dis., 24: 1-13.
Rhouma, M; Beaudry, F and Letellier, A (2016). Resistance to colistin: what is the fate for this antibiotic in pig production? Int. J. Antimicrob. Agents. 48: 119-126.
Ribeiro, S; Mourão, J; Novais, Â; Campos, J; Peixe, L and Antunes, P (2021). From farm to fork: Colistin voluntary withdrawal in Portuguese farms reflected in decreasing occurrence of mcr-1-carrying Enterobacteriaceae from chicken meat. Environ. Microbiol., 121: 234-247.
Sabala, RF; Usui, M; Tamura, Y; Abd-Elghany, SM; Sallam, KI and Elgazzar, MM (2021). Prevalence of colistin-resistant Escherichia coli harbouring mcr-1 in raw beef and ready-to-eat beef products in Egypt. Food Control. 119: 107436-107445.
Sadeghi Dosari, A; Norouzi, A; Taati Moghadam, M and Satarzadeh, N (2016). Antimicrobial activity of Ephedra pachyclada methanol extract on some enteric gram negative bacteria which causes nosocomial infections by agar dilution method. Zahedan. J. Res. Med. Sci., 18: 21-29.
Sadek, M; Ortiz De La Rosa, JM; Abdelfattah Maky, M; Korashe Dandrawy, M; Nordmann, P and Poirel, L (2021). Genomic features of MCR-1 and extended-spectrum β-lactamase-producing Enterobacterales from retail raw chicken in Egypt. Microorganisms. 9: 195-208.
Savin, M; Bierbaum, G; Schmithausen, RM; Heinemann, C; Kreyenschmidt, J; Schmoger, S; Akbaba, I; Käsbohrer, A and Hammerl, JA (2022). Slaughterhouse wastewater as a reservoir for extended-spectrum β-lactamase (ESBL)-producing, and colistin-resistant Klebsiella spp. and their impact in a “One Health” perspective. Sci. Total Environ., 804: 150000-150012.
Shafiq, M; Rahman, SU; Bilal, H; Ullah, A; Noman, SM; Zeng, M; Yuan, Y; Xie, Q; Li, X and Jiao, X (2022). Incidence and molecular characterization of ESBL-producing and colistin-resistant Escherichia coli isolates recovered from healthy food-producing animals in Pakistan. J. Appl. Microbiol., 53: 117-125.
Shahbandeh, M; Moghadam, MT; Mirnejad, R; Mirkalantari, S and Mirzaei, M (2020). The efficacy of AgNO3 nanoparticles alone and conjugated with imipenem for combating extensively drug-resistant Pseudomonas aeruginosa. J. Nanomed. Res., 15: 6905-6917.
Shariati, A; Dadashi, M; Moghadam, MT; Van Belkum, A; Yaslianifard, S and Darban-Sarokhalil, D (2020). Global prevalence and distribution of vancomycin resistant, vancomycin intermediate and heterogeneously vancomycin intermediate Staphylococcus aureus clinical isolates: a systematic review and meta-analysis. Sci. Rep., 10: 1-16.
Shi, X; Li, Y; Yang, Y; Shen, Z; Cai, C; Wang, Y; Walsh, TR; Shen, J; Wu, Y and Wang, S (2021). High prevalence and persistence of carbapenem and colistin resistance in livestock farm environments in China. J. Hazard. Mater., 406: 124298-124306.
Sismova, P; Sukkar, I; Kolidentsev, N; Palkovicova, J; Chytilova, I; Bardon, J; Dolejska, M and Nesporova, K (2023). Plasmid-mediated colistin resistance from fresh meat and slaughtered animals in the Czech Republic: nation-wide surveillance 2020-2021. Microbiol. Spectr., 11: e00609-e00623.
Stewart, PS (2002). Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol., 292: 107-113.
Sun, J; Zhang, H; Liu, YH and Feng, Y (2018). Towards understanding MCR-like colistin resistance. Trends. Microbiol., 26: 794-808.
Taati Moghadam, M; Hossieni Nave, H; Mohebi, S and Norouzi, A (2016). The evaluation of connection between integrons class I and II and ESBL-producing and Non-ESBL klebsiella pneumoniae isolated from clinical samples, Kerman. Iran. J. Med. Microbiol., 10: 1-9.
Taati Moghadam, M; Mirzaei, M; Fazel Tehrani Moghaddam, M; Babakhani, S; Yeganeh, O; Asgharzadeh, S; Farahani, HE and Shahbazi, S (2021). The challenge of global emergence of novel colistin-resistant Escherichia coli ST131. Microb. Drug Resist., 27: 1513-1524.
Tartor, YH; Gharieb, R; El-Aziz, A; Norhan, K; El Damaty, HM; Enany, S; Khalifa, E; Attia, AS; Abdellatif, SS and Ramadan, H (2021). Virulence determinants and plasmid-mediated colistin resistance mcr genes in Gram-negative bacteria isolated from bovine milk. Front. Cell. infect. Microbiol., 11: 761417-761425.
Uruén, C; Chopo-Escuin, G; Tommassen, J; Mainar-Jaime, RC and Arenas, J (2021). Biofilms as promoters of bacterial antibiotic resistance and tolerance. Antibiotics. 10: 3-11.
Valiakos, G and Kapna, I (2021). Colistin resistant mcr genes prevalence in livestock animals (swine, bovine, poultry) from a multinational perspective. A systematic review. J. Vet. Sci., 8: 265-277.
Wang, X; Wang, Y; Zhou, Y; Li, J; Yin, W; Wang, S; Zhang, S; Shen, J; Shen, Z and Wang, Y (2018). Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg. Micro. Infec., 7: 1-9.
Wang, Y; Xu, C; Zhang, R; Chen, Y; Shen, Y; Hu, F; Liu, D; Lu, J; Guo, Y and Xia, X (2020). Changes in colistin resistance and mcr-1 abundance in Escherichia coli of animal and human origins following the ban of colistin-positive additives in China: an epidemiological comparative study. Lancet Infect. Dis., 20: 1161-1171.
Wi, YM; Choi, JY; Lee, JY; Kang, CI; Chung, DR; Peck, KR; Song, JH and Ko, KS (2017). Emergence of colistin resistance in Pseudomonas aeruginosa ST235 clone in South Korea. Int. J. Antimicrob. Agents. 49: 767-769.
Xavier, BB; Lammens, C; Ruhal, R; Kumar-Singh, S; Butaye, P; Goossens, H and Malhotra-Kumar, S (2016). Identification of a novel plasmid-mediated colistin-
resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill., 21: 30280-30287.
Xiong, W; Wang, Y; Sun, Y; Ma, L; Zeng, Q; Jiang, X; Li, A; Zeng, Z and Zhang, T (2018). Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes. Microbiome. 6: 1-11.
Yang, YQ; Li, YX; Lei, CW; Zhang, AY and Wang, HN (2018). Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. J. Antimicrob. Chemother., 73: 1791-1795.
Yassin, AK; Zhang, J; Wang, J; Chen, L; Kelly, P; Butaye, P; Lu, G; Gong, J; Li, M and Wei, L (2017). Identification and characterization of mcr mediated colistin resistance in extraintestinal Escherichia coli from poultry and livestock in China. FEMS Microbiol. Lett., 364: fnx242-fnx251.
Yin, W; Li, H; Shen, Y; Liu, Z; Wang, S; Shen, Z; Zhang, R; Walsh, TR; Shen, J and Wang, Y (2017). Novel plasmid-mediated colistin resistance gene mcr-3 in Escherichia coli. Mbio. 8: e00543-e00617.
Zhang, S; Huang, Y; Yang, G; Lei, T; Chen, M; Ye, Q; Wang, J; Gu, Q; Wei, X and Zhang, J (2021). High prevalence of multidrug-resistant Escherichia coli and first detection of IncHI2/IncX4-plasmid carrying mcr-1 E. coli in retail ready-to-eat foods in China. Int. J. Food Microbiol., 355: 109349-109356.
Zhang, X; Zhang, B; Guo, Y; Wang, J; Zhao, P; Liu, J and He, K (2019). Colistin resistance prevalence in Escherichia coli from domestic animals in intensive breeding farms of Jiangsu Province. Int. J. Food Microbiol., 291: 87-90.

Files

Share

How to cite

Statistics